Skip to main content
SpringerLink
Log in

Dynamics of circulating lipoproteins and lipids in Brown Skua (Stercorarius antarcticus lonnbergi) during the breeding cycle

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

In central-place foragers the breeding cycle is often the period with the highest energy cost, where dietary and stored lipids play a key role. Lipids are mobilized through blood lipoproteins providing fuel to tissues. Thus, the use of food and endogenous resources with high-energy fats is important to sustain individuals’ nutritional demands. To evaluate the physiological components associated to energetic demands and their variation regarding life history processes, we analysed the plasma circulating lipoprotein levels, the lipid classes and fatty acid (FA) composition in Brown Skua (Stercorarius antarcticus lonnbergi) in breeding stages with different energy requirements: incubation (In), early rearing (Er) and late rearing (Lr). We expected to find differences according to the energy demands of each stage and the sex. The level of Very Low Density lipoproteins was affected by the sex and the breeding stage, whereas Low Density lipoproteins only by the stage. Total plasma lipid content and circulating lipid classes were invariant among the stages studied; however, differences in total plasma FA and monounsaturated FA (oleic and nervonic) abundances were observed among stages. Besides, a decrease in the n-3:n-6 ratio was observed towards the Lr stage. The differences found in lipoproteins may be linked to changes in the energy demands throughout the breeding period. Moreover, the variation observed in FA abundance and n-3:n-6 ratio may be related to a preferential mobilization of FA from stores as fuel or, possibly, to a differential use of the available food resources.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aguirre CA (1995) Distribution and abundance of birds at Potter Peninsula, 25 de Mayo (King George) Island, South Shetland Islands, Antarctica. Marine Ornithol 23:23–31

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) lme4: Linear mixed effects models using Eigen and S4. R package version 1.1.8. http://CRAN.Rproject.org/package=lme4.

  • Baylin A, Campos H (2006) The use of fatty acid biomarkers to reflect dietary intake. Curr Opin Lipidol 17(1):22–27

    Article  CAS  PubMed  Google Scholar 

  • Bentzen RL, Powell AN, Williams TD, Kitaysky AS (2008) Characterizing the nutritional strategy of incubating king eiders Somateria spectabilis in northern Alaska. J Avian Biol 39:683–690

    Article  Google Scholar 

  • Blem CR (1990) Avian energy storage Curr Ornithol 7:59–113

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917

    Article  CAS  PubMed  Google Scholar 

  • Borghello P, Torres DS, Montalti D, Ibañez AE (2018) Diet of the Brown Skua (Stercorarius antarcticus) at Hope Bay, Antarctic Peninsula: differences between breeders and non-breeders. Polar Biol 42:385–394

    Article  Google Scholar 

  • Bourgeon S, Le Maho Y, Raclot T (2009) Proximate and ultimate mechanisms underlying immunosuppression during the incubation fast in female eiders: Roles of triiodothyronine and corticosterone. Gen Comp Endocrinol 163(1–2):77–82

    Article  CAS  PubMed  Google Scholar 

  • Bourgeon S, Kauffmann M, Geiger S, Raclot T, Robin JP (2010) Relationships between metabolic status, corticosterone secretion and maintenance of innate and adaptive humoral immunities in fasted re-fed mallards. J Exp Biol 213(Pt 22):3810–3818

    Article  CAS  PubMed  Google Scholar 

  • Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22(4):759–801

    Article  Google Scholar 

  • Burton RW (1968) Breeding Biology of the Brown Skua Catharacta skua lonnbergi (Mathews), at Signy Island, Soth Orkney Islands. Br Antarct Surv Bull 15:9–28

    Google Scholar 

  • Carrascal LM, Senar JC, Mozetich I, Uribe F, Domenech J (1998) Interactions among environmental stress, body condition, nutritional status, and dominance in great tits. Auk 115:727–738

    Article  Google Scholar 

  • Cerasale DJ, Guglielmo CG (2006) Dietary effects on prediction of body mass changes in birds by plasma metabolites. Auk 123(3):836–846

    Article  Google Scholar 

  • Conway CJ, Eddleman WR, Simpson KL (1994) Seasonal changes in fatty acid composition of the Wood Thrush. Condor 96(3):791–794

    Article  Google Scholar 

  • Cooper MH, Iverson SJ, Heras H (2005) Dynamics of blood chylomicron fatty acids in a marine carnivore: implications for lipid metabolism and quantitative estimation of predator diets. J Comp Physiol B 175(2):133–145

    Article  CAS  PubMed  Google Scholar 

  • Davis RA (1997) Evolution of processes and regulators of lipoprotein synthesis: From Birds to Mammals. J Nutr 127:795S-800S

    Article  CAS  PubMed  Google Scholar 

  • Devillers P (1978) Distribution and relationships of South American Skuas. Gerfaut 68:374–417

    Google Scholar 

  • Feng Y, Ding Y, Liu J, Tian Y, Yang Y, Guan S, Zhang C (2015) Effects of dietary omega-3/omega-6 fatty acid ratios on reproduction in the young breeder rooster. BMC Vet Res 11:73

    Article  PubMed  PubMed Central  Google Scholar 

  • Furness RW (1987) The skuas. A.D. Poyser, Calton

    Google Scholar 

  • Graña Grilli M, Montalti D (2012) Trophic interactions between Brown and South Polar Skuas at Deception Island. Antarctica Polar Biol 35(2):299–304

    Article  Google Scholar 

  • Graña Grilli M, Marti LJ, Montalti D (2014) Uniformity of diet composition of Brown Skuas at different ages and between siblings. Rev Bras Ornitol 22:265–269

    Article  Google Scholar 

  • Graña Grilli M, Montalti D (2015) Variation in diet composition during the breeding cycle of an Antarctic seabird in relation to its breeding chronology and that of its main food resource. Polar Biol 38(5):643–649

    Article  Google Scholar 

  • Graña Grilli M, Pari M, Ibañez AE (2018) Poor body conditions during the breeding period of a low breeding success seabird population. Marine Biol 165:142

    Article  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7(8):1071–1075

    Article  CAS  PubMed  Google Scholar 

  • Groscolas R, Robin JP (2001) Long-term fasting and re-feeding in penguins. Comp Biochem Physiol A Mol Integr Physiol 128:645–655

    Article  CAS  PubMed  Google Scholar 

  • Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002a) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a long-distance migrant shorebird. Am J Physiol 282(5):1405-R1413

    Google Scholar 

  • Guglielmo CG, Williams TD, Zwingelstein G, Brichon G, Weber JM (2002b) Plasma and muscle phospholipids are involved in the metabolic response to long-distance migration in a shorebird. J Comp Physiol B 172(5):409–417

    Article  CAS  PubMed  Google Scholar 

  • Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2005) Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc R Soc Lond B 272(1657):1039–1046

    Google Scholar 

  • Heras H, Gonzalez-Baró M, Pollero RJ (2000) Lipid and fatty acid composition and energy partitioning during embryo development in the shrimp Macrobrachium borellii. Lipids 35(6):645–651

    Article  CAS  PubMed  Google Scholar 

  • Hermier D, Chapman MT, Leaclercq B (1984) Plasma lipoprotein profile in fasted and refed chickens of two strains selected for high or low adiposity. J Nutr 114(6):1112–1121

    Article  CAS  PubMed  Google Scholar 

  • Hermier D (1997) Lipoprotein metabolism and fattening in poultry. J Nutr 127:805S-808S

    Article  CAS  PubMed  Google Scholar 

  • Hollmén T, Franson JC, Hario M, Sankari S, Kilpi M, Lindstrom K (2000) Use of serum biochemistry to evaluate nutritional status and health of incubating common eiders (Somateria mollissima) in Finland. Physiol Biochem Zool 74:333–342

    Article  Google Scholar 

  • Ibañez A, Graña Grilli M, Figueroa A, Pari M, Montalti D (2018) Declining health status of Brown Skua (Stercorarius antarcticus lonnbergi) parents and their offspring during chick development. Polar Biol 41(1):193–200

    Article  Google Scholar 

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: A new method of estimating predator diets. Ecol Monogr 74(2):211–235

    Article  Google Scholar 

  • Jenni-Eiermann S, Jenni L (1992) High plasma triglyceride levels in small birds during migratory flight: a new pathway for fuel supply during endurance locomotion at very high mass-specific metabolic rates? Physiol Zool 65(1):112–123

    Article  CAS  Google Scholar 

  • Jenni-Eiermann S, Jenni L (1998) What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biol Cons Fauna 102:312–319

    Google Scholar 

  • Käkelä R, Käkelä A, Kahle S, Becker PH, Kelly A, Furness RW (2005) Fatty acid signatures in plasma of captive herring gulls as indicators of demersal or pelagic fish diet. Mar Ecol Prog Ser 293:191–200

    Article  Google Scholar 

  • Käkelä A, Crane J, Votier SC, Furness RW, Käkelä R (2006) Fatty acid signatures as indicators of diet in great skuas Stercorarius skua, Shetland. Mar Ecol Prog Ser 319:297–310

    Article  Google Scholar 

  • Käkelä R, Furness RW, Kahle S, Becker PH, Käkelä A (2009) Fatty acid signatures in seabird plasma are a complex function of diet composition: a captive feeding trial with herring gulls. Funct Ecol 23(1):141–149

    Article  Google Scholar 

  • Klasing KC (1998) Comparative Avian Nutrition. CAB International, New York

    Book  Google Scholar 

  • Krietsch J, Hahn S, Kopp M, Phillips RA, Peter HU, Lisovski S (2017) Consistent variation in individual migration strategies of Brown Skuas. Mar Ecol Prog Ser 578:213–225

    Article  Google Scholar 

  • Lormée H, Jouventin P, Trouve C, Chastel O (2003) Sex-specific patterns in baseline corticosterone and body condition changes in breeding Red-footed Boobies Sula sula. Ibis 145:212–219

    Article  Google Scholar 

  • McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35(5):377–393

    Article  Google Scholar 

  • Mitchell GW, Wheelwright NT, Guglielmo CG, Norris DR (2012) Short-and long-term costs of reproduction in a migratory songbird. Ibis 154(2):325–337

    Article  Google Scholar 

  • Morrison WR, Smith LM (1992) Preparation of fatty acid methyl esters and dimethylacetals from lipid with boron fluoride-methanol. J Lipid Res 5:600–608

    Article  Google Scholar 

  • Navidshad B, Deldar H, Pourrahimi G (2010) Correlation between serum lipoproteins and abdominal fat pad in broiler chickens. Afr J Biotechnol 9(35):5779–5783

    CAS  Google Scholar 

  • Noble R (1968) Electrophoretic separation of plasma lipoproteins in agarose gel. J Lipid Res 9(6):693–700

    Article  CAS  PubMed  Google Scholar 

  • Peebles ED, Burnham MR, Walzem RL, Branton SL, Gerard PD (2004) Effects of fasting on serum lipids and lipoprotein profiles in the egg-laying hen (Gallus domesticus). Comp Biochem Physiol A Mol Integr Physiol 138(3):305–311

    Article  CAS  PubMed  Google Scholar 

  • Pierce BJ, McWilliams SR (2005) Seasonal changes in composition of lipid stores in migratory birds: causes and consequences. Condor 107(2):269–279

    Article  Google Scholar 

  • Pierce BJ, McWilliams SR, O´Connor T, Place AR, Guglielmo C, (2005) Effect of dietary fatty acid composition on depot fat and exercise performance in a migrating songbird, the Red-eyed Vireo. J Exp Biol 208(Pt 7):1277–1285

    Article  CAS  PubMed  Google Scholar 

  • Polito MJ, Koopman HN, Able S, Walsh J, Goebel ME (2012) Physiological constraints and the influence of diet on fatty acids in the yolk of gentoo penguins. Pygoscelis papua J Comp Physiol B 182(5):703–713

    Article  CAS  PubMed  Google Scholar 

  • Price ER, Krokfors A, Guglielmo GC (2008) Selective mobilization of fatty acids from adipose tissue in migratory birds. J Exp Biol 211(11):29–34

    Article  CAS  PubMed  Google Scholar 

  • Price ER, Guglielmo CG (2009) The effect of muscle phospholipid fatty acid composition on exercise performance: a direct test in the migratory white-throated sparrow (Zonotrichia albicollis). Am J Physiol 297:R775–R782

    CAS  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http:// www.R-project.org/

  • Raclot T (2003) Selective mobilization of fatty acids from adipose tissue triglycerides. Prog Lipid Res 42(4):257–288

    Article  CAS  PubMed  Google Scholar 

  • Ramenofsky M (1990) Fat storage and fat metabolism in relation to migration. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer, Berlin Heidelberg, pp 214–231

    Chapter  Google Scholar 

  • Reinhardt SB, Van Vleet ES (1986) Lipid composition of twenty-two species of Antarctic midwater zooplankton and fish. Marine Biol 91:149–159

    Article  CAS  Google Scholar 

  • Ritz M, Millar C, Miller G, Phillips R, Ryan P, Sternkopf V, Liebers-Helbig D, Peter HU (2008) Phylogeography of the southern Skua complex- rapid colonization of the southern hemisphere during a glacial period and reticulate evolution. Mol Phylogenet Evol 49(1):292–303

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touchstone JC, Levin SS, Dobbins MF, Beers PC (1983) Analysis of saturated and unsaturated phospholipids in biological fluids. J Liq Chrom 6(1):179–192

    Article  CAS  Google Scholar 

  • Twining CW, Brenna JT, Lawrence P, Shipley JR, Tollefson TN, Winkler DW (2016) Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity. PNAS 113:39

    Article  Google Scholar 

  • Tveraa T, Saether BE, Aanes R, Erikstad KE (1998) Body mass and parental decisions in the Antarctic petrel Thalassoica antarctica: how long should the parents guard the chick? Behav Ecol Sociobiol 43(2):73–79

    Article  Google Scholar 

  • Votier SC, Bearhop S, Ratcliffe N, Furness RW (2001) Pellets as indicators of diet in Great Skuas Catharacta skua. Bird Study 48(3):373–376

    Article  Google Scholar 

  • Wathes DC, Abayasekara DR, Aitken RJ (2007) Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77(2):190–201

    Article  CAS  PubMed  Google Scholar 

  • Weimerskirch H (1990) Weight loss of Antarctic Fulmars Fulmarus glacialoides during incubation and chick brooding. Ibis 132(1):68–77

    Article  Google Scholar 

  • Williams TD (2005) Mechanisms underlying the costs of egg production. Bioscience 55(1):39–48

    Article  Google Scholar 

  • Williams CT, Buck CL (2010) Using fatty acids as dietary tracers in seabird trophic ecology: theory, application and limitations. J Ornithol 151(3):531–543

    Article  Google Scholar 

  • Zuur A, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, New York, USA

    Book  Google Scholar 

Download references

Acknowledgements

This work was made possible thanks to National Office of the Antarctic (DNA) and Argentine Antarctic Institute (IAA) which provided logistical support to carry out the fieldwork at Potter Peninsula, Isla 25 de Mayo/ King George Island, South Shetland Islands, Antarctica. This work was supported by Proyecto de Investigación Plurianual (PIP- CONICET n° 0158) and Agencia Nacional de Promoción Científica y Tecnológica and Instituto Antártico Argentino (PICTA-2010-0080) (To DM), and partially supported by (PICT-2014-3323) (to AEI). Special thanks to Facundo Xavier Palacio for the help with statistical analysis and to Rosana del Cid for the help with manuscript writing and grammatical edition, as well as to the Editor and reviewers for their interesting and helpful critics for the improvement of the manuscript.

Author information

Authors and Affiliations

  1. Sección Ornitología, División Zoología Vertebrados, Museo de La Plata, Facultad de Ciencias Naturales Y Museo, Universidad Nacional de La Plata, B1900FWA, La Plata, Buenos Aires, Argentina

    A. E. Ibañez & D. Montalti

  2. Instituto de Investigaciones Bioquímicas de La Plata (INIBIOLP), CONICET, Universidad Nacional de La Plata, La Plata, Argentina

    M. Y. Pasquevich & H. Heras

  3. Departamento de Bioquímica Clínica, Facultad de Farmacia Y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina

    N. Fernandez Machulsky & G. Berg

  4. Instituto Antártico Argentino (IAA), San Martín, Buenos Aires, Argentina

    D. Montalti

  5. Grupo de Investigaciones en Biología de La Conservación, Laboratorio Ecotono, INIBIOMA, CONICET, Universidad Nacional del Comahue, Bariloche, Argentina

    M. Graña Grilli

Authors
  1. A. E. Ibañez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Y. Pasquevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Fernandez Machulsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Heras
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. Montalti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Graña Grilli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AEI was involved in the design of the fieldwork activities, performed experiments and prepared the manuscript, PMY and HH were involved in experimental design of with lipid analysis and provided reactives, FMN and BG were involved in lipoprotein analysis, DM and MGG were involved in the design and founding of project, conducted the fieldwork activities and collaborated with the edition of the manuscript.

Corresponding author

Correspondence to A. E. Ibañez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The permit to carry out the fieldwork for this work was given by National Office of the Antarctic (DNA). All applicable international, national, and institutional guidelines for sampling, care, and experimental use of animals for the study were followed as established by the Article III, Annex II of the Madrid Protocol, Law 24.216 (Taking, Harmful Intrusion and Introduction of Species) within the framework of the projects evaluated by the Environment Office of the Argentine Antarctic Institute (IAA) and DNA.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ibañez, A.E., Pasquevich, M.Y., Machulsky, N.F. et al. Dynamics of circulating lipoproteins and lipids in Brown Skua (Stercorarius antarcticus lonnbergi) during the breeding cycle. Polar Biol 44, 305–314 (2021). https://doi.org/10.1007/s00300-020-02793-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-020-02793-1

Keywords

Search

Navigation